Critical Reviews in Plant Sciences

ISSN: 0735-2689 (Print) 1549-7836 (Online) Journal homepage: http://www.tandfonline.com/loi/bpts20

Patterns and Mechanisms of Nutrient Resorption

in Plants

Amber N. Brant & Han Y.H. Chen

To cite this article: Amber N. Brant & Han Y.H. Chen (2015) Patterns and Mechanisms
of Nutrient Resorption in Plants, Critical Reviews in Plant Sciences, 34:5, 471-486, DOI:
10.1080/07352689.2015.1078611

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 Critical Reviews in Plant Sciences, 34:471–486, 2015
Copyright Ó Taylor & Francis Group, LLC
ISSN: 0735-2689 print / 1549-7836 online
DOI: 10.1080/07352689.2015.1078611

Patterns and Mechanisms of Nutrient Resorption in Plants

Amber N. Brant and Han Y.H. Chen

Faculty of Natural Resources Management, Lakehead University, Thunder Bay, Canada

Table of Contents

I. INTRODUCTION........................................................................................................................................ 472

II. PLANT NUTRIENT USE AND RESORPTION ............................................................................................. 472

A. Plant Nutrient Use and Stoichiometry........................................................................................................ 472
B. Resorption as a Nutrient Conservation Strategy .......................................................................................... 473
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III. NUTRIENT RESORPTION AMONG PLANT TISSUES ................................................................................ 474

A. Leaves ................................................................................................................................................. 474
B. Stems................................................................................................................................................... 475
C. Fine Roots ............................................................................................................................................ 475

IV. CONTROLS OF GENETIC VARIABILITY.................................................................................................. 475

A. Variation among Plant Life-Forms............................................................................................................ 477
1. Woody plants .................................................................................................................................. 477
2. Graminoids and other non-woody plants.............................................................................................. 477
B. Role of Leaf Habit ................................................................................................................................. 477

V. CONTROLS OF TIME AND PLANT DEVELOPMENT ................................................................................ 478

VI. ENVIRONMENTAL CONTROLS ................................................................................................................ 479

A. Climate ................................................................................................................................................ 479
1. Latitude and climate variables............................................................................................................ 479
2. Climate change................................................................................................................................ 479
B. Soil Fertility.......................................................................................................................................... 480

VII. SUMMARY AND FUTURE PERSPECTIVES ............................................................................................... 481

ACKNOWLEDGMENTS .................................................................................................................................... 482

REFERENCES.................................................................................................................................................... 482

non-leaf plant tissues for whole-plant nutrient budget accounting,

Nutrient resorption (NR) plays a key role in the nutrient
conservation of plants. However, a fundamental understanding of
the mechanisms that control NR remains limited. In this review,
we examine how intrinsic controls (e.g., genetic variability and
plant development) and extrinsic environmental controls (e.g.,
climate and soil fertility) influence NR. We also examined
conceptual NR advances, mass loss correction, measurement in
and the use of stoichiometric ratios in place of individual
elements. Nutrient resorption from senescing leaves is greater
than that from stems/culms or roots. Nutrients resorbed from
stems and roots in woody plants are lower than in non-woody
plants. Deciduous plants are more efficient in resorbing leaf
nutrients prior to senescence than are evergreen plants.
Furthermore, reproductive efforts tend to increase NR. Along a
latitudinal gradient of terrestrial biomes, nitrogen resorption

Address correspondence to Han Y.H. Chen, Faculty of Natural Resources Management, Lakehead University, 955 Oliver Road, Thunder
Bay, ON P7B 5E1, Canada. E-mail: hchen1@lakeheadu.ca.

471
 472 A. N. BRANT AND H. Y. H. CHEN
efficiency decreases and phosphorus resorption efficiency
increases with increasing temperature and precipitation;
however, latitudinal patterns reflect the influences of several
coupling factors such as genetic variation, climate, soil, and
disturbance history. Nutrient fertilization experiments have
demonstrated that increased soil fertility reduces NR. The
inquiries into the impacts of ongoing climate change on NR are
still at a nascent stage. Future NR studies are needed to better
understand the independent effects of a wide range of genetic
variation, plant development, and environment, and possibly the
different responses of plants to environmental change;
particularly elevated atmospheric CO2 concentrations and global
warming.
Keywords climate, leaf chemistry, leaf habit, meta-analysis, nutri-
ent conservation, nutrient resorption, plant life-forms,
plant nutrition, soil fertility, stoichiometry
I. INTRODUCTION
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The mobilization and use of nutrients by plant communities
have captivated the attention of researchers for almost a cen-
tury (Combes, 1926; Williams, 1955; Vitousek, 1982; Attiwill
and Adams, 1993). Nutrient resorption (NR) allows for the
conservation of nutrients that may be otherwise lost to soils
via litterfall following senescence (Aerts and Chapin, 2000).
The most recent global estimate for the average percentage of
nutrients that are resorbed back into live plant tissues are
62.1% for N and 64.9% for P (Vergutz et al., 2012; Figure 1).
When the NR process is artificially prevented, plant fitness
traits, such as biomass increment growth, stem growth, and
fruit production, are adversely affected (May and Killingbeck,
1992). Improving our knowledge of NR may provide a great
deal of information regarding nutrient use strategies.
The initial two reviews on the topic of NR placed their
emphasis on the physiological mobility of nutrients throughout
phloem tissues (Loneragan et al., 1976; Hill, 1980). At this
time, interest in NR was focussed more on physiological
FIG. 1. Percentage of nitrogen (N) and phosphorus (P) resorbed back into live
tissues and inputs into the soil via litterfall during leaf senescence from global
estimates (Vergutz et al., 2012). Question marks are for plant tissues with no
global estimate.
constraints (Chapin, 1980), and it was not until the review by
Aerts (1996) that the effects of soil fertility and interspecific
variation on NR were addressed. In this review, no evidence
for a connection between soil fertility and NR was found, and
it was argued that NR is not reflected in green leaf nutrient
concentrations (Aerts, 1996). Building on previously pub-
lished concepts, Aerts and Chapin (2000) then published a
review on NR in the context of variation across plant func-
tional types and soil fertility, which focused on the variation
of plant strategies with nutrient use and cycling. Since then,
many studies have provided both positive and contradictory
evidence for these null claims (Eckstein et al., 1999; Diehl
et al., 2003; Yuan et al., 2005b; Yuan and Chen, 2009a), sup-
ported by increased efforts with global syntheses and updated
research methods (Vergutz et al., 2012; Yuan and Chen,
2015b). Despite the increased focus on plant functional traits
and their effects on NR and nutrient cycling (Killingbeck and
Tainsh, 2002; Escudero and Mediavilla, 2003; Wright and
Westoby, 2003; Ordonez et al., 2009; Fujita et al., 2013;
Zhang et al., 2013), there has not been a critical review since
Aerts and Chapin (2000) that addresses the effects of plant
growth forms on NR. Furthermore, there has been no critical
review on the effects of climate and plant developmental
stages on NR, nor for observations among non-leaf plant tis-
sues, which is a new parameter in this field of study.
The way that perennial plants retranslocate nutrients back
into living tissues is influenced by leaf habit (Aerts, 1995; Lal
et al., 2001), development stage (Milla et al., 2005; Yuan and
Chen, 2010a; Ye et al., 2012; Tully et al., 2013), soil fertility
(Yuan et al., 2006; Drenovsky et al., 2013; Yuan and Chen,
2015b), and climatic factors (Oleksyn et al., 2003; Yuan and
Chen, 2009a). While there have been advances toward improv-
ing our understanding of plant nutrients, specifically nutrient
recycling in plants, questions still remain to be addressed as
relates to how NR may differ among plant tissues and how
genetic variability, development, and environment control NR
in plants. For this review, we have developed a general con-
ceptual framework of how NR is influenced by genetic vari-
ability, development, and environment (Figure 2). We begin
with a description of plant nutrient use and NR as a strategy
for nutrient conservation and then discuss the structural con-
trols on NR, specifically observations in different plant tissues.
Variations in the genetic expression of NR in the context of
plant life forms and leaf habit are further examined. We inves-
tigate how NR changes with plant development, at both the
plant and ecosystem levels, and finally, address the environ-
mental controls that drive NR variations in plants.
II. PLANT NUTRIENT USE AND RESORPTION
A. Plant Nutrient Use and Stoichiometry
The importance of nutrient use and cycling in plant ecosys-
tems cannot be underestimated, given that plants require
 NUTRIENT RESORPTION IN PLANTS
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FIG. 2. Conceptual model of controls of nutrient resorption in plants (solid
arrows) and interactions between the controls (dashed arrows).
sufficient amounts of biologically available nutrients to sup-
port growth, survival, and reproduction. Essential nutrients for
plant functionality include carbon (C), nitrogen (N), phospho-
rus (P), potassium (K), calcium (Ca), magnesium (Mg), among
other elements. Nutrients are first introduced to the soil from
either biological or parent material sources (Aerts and Chapin,
2000). Primary influxes of N are derived from the atmosphere
through deposition, whereas P derives from rock weathering
(Aerts and Chapin, 2000). Once in the soil, nutrients are taken
up by plants, which is facilitated by mycorrhizae and/or nitro-
gen-fixing bacteria that are found within the soil environment
(Aerts and Chapin, 2000). At the cellular level, N is primarily
utilized by plants for enzymatic activity and to enable photo-
synthesis (Evans, 1989), while also playing an essential role in
the mobilization and storage of other key nutrients (Canton
et al., 2005). Phosphorus is employed for energy transfer
(Aerts and Chapin, 2000) and metabolism (Vance et al.,
2003).
A fundamental focus of plant nutrient research is limitation
– a metric classically recognized as the requirement of a given
nutrient for plant growth, reproduction, and survival (Chapin,
1980). Many studies on nutrient limitation divide land forms
between terrestrial and marine environments (Vitousek and
Howarth, 1991), concentrating on either single elements (Aber
et al., 1998; de Campos et al., 2013), or ratios between ele-
ments (Koerselman and Meuleman, 1996; G€ usewell, 2004).
Two macronutrients (N and P) have received the most atten-
tion in plant nutrient studies, primarily due to their close rela-
tionship with plant growth (Attiwill and Adams, 1993; Aerts
and Chapin, 2000), and therefore the most limiting in terres-
trial environments (Chapin, 1980). The differences in influx
between these two macronutrients may explain the variations
473
in nutrient limitation among biomes. Net primary production
of all photosynthetic organisms is limited by N (Vitousek and
Howarth, 1991) in both aboveground (LeBauer and Treseder,
2008) and belowground (Yuan and Chen, 2012b) environ-
ments, whereas P-limitation is more apparent in the tropics
than other biomes (Yuan and Chen, 2012b). The irreversible
binding of P with clay soils without weathering renders it
unavailable for plant mobilization (Vitousek, 1984). Growth
in boreal and temperate plants, however, tends to be more N-
limited because of N losses due to leaching and denitrification
into the atmosphere from frequent fire events and lower tem-
peratures (Bonan and Shugart, 1989; Aber et al., 1998; Aerts
and Chapin, 2000).
Interest in nutrient limitation of plant communities has
shifted from the limitation of single nutrients (Williams, 1955;
Vitousek, 1982) to factors that affect nutrient co-limitation at
large spatial scales (Harpole et al., 2011; Fisher et al., 2012;
Yuan and Chen, 2012b) and long temporal scales (Menge
et al., 2012). Nutrient stoichiometry in biological communities
was first introduced by Alfred C. Redfield in the early 1930s,
who developed and published a set of chemical constraints for
C, N, and P on the biomass production of planktonic organ-
isms in marine environments (Redfield, 1934). Since then, C:
N:P ratios in the sea have been translated for applications in
terrestrial environments (McGroddy et al., 2004). The updated
C:N:P ratio for plant foliage by mass using Redfield numbers
is 1212:28:1, whereas the ratio for plant litter is 3007:45:1
(McGroddy et al., 2004), and that for plant fine roots (<2 mm
in diameter) is 906:15:1 (Yuan et al., 2011). Stoichiometry is
becoming a more important aspect of plant nutrition because
of the inherent relationships between essential elements and
plant growth (Elser et al., 2003), making Liebig’s classical
Law of the Minimum (Danger et al., 2008) practically obso-
lete. A main focus of research in plant nutrient dynamics today
is the flexibility of stoichiometric relationships in terrestrial
environments (Yuan et al., 2011; Agren and Weih, 2012; Sis-
tla and Schimel, 2012) due to the intensifying interest in global
ecosystem changes (Aerts et al., 2012; Austin and Vitousek,
2012; Sardans and Penuelas, 2012; Yuan and Chen, 2015a).
B. Resorption as a Nutrient Conservation Strategy
Nutrient resorption plays a significant role in maintaining a
balance in the stoichiometry of plants. Classically named
“backmigration” (Fries, 1952), “redistribution” (Williams,
1955), “retranslocation” (Chapin, 1980), “remobilization” (Hill,
1980), or “reabsorption or resorption” (Jonasson, 1989), among
others, NR is most succinctly defined as the movement of
nutrients in photosynthetic organisms from senescing tissues
back to surviving tissues (Killingbeck, 1986). This definition
has since been expanded to include nutrient resorption profi-
ciency, the terminal concentration of a given nutrient in sen-
esced tissue as a proxy for resorption potential defined as
complete, intermediate, or incomplete (Killingbeck, 1996), and
 474 A. N. BRANT AND H. Y. H. CHEN
the transfer from old, but still live, plant tissues to new sink tis-
sues (Nambiar and Fife, 1991; Freschet et al., 2010; Mao et al.,
2013). Interest in NR within the field of plant biology has been
expanding since the early 20th century (Combes, 1926;
McHargue and Roy, 1932) with an increased occupation with
fertilization (Goodman et al., 2014; Mayor et al., 2014; Wang
et al., 2014) and nutrient limitation (Han et al., 2013).
Nutrient resorption is different from passive nutrient leach-
ing from one plant organ to another (Hagen-Thorn et al.,
2006). Passive leaching allows for nutrient escape into the
atmosphere or an aqueous body, in which the organ being sub-
merged or in heavy rainfall induces leaching (Long et al.,
1956; Tukey Jr, 1970). Resorbed nutrients are actively trans-
ported via phloem through abscission zones (Williams, 1955;
Chapin, 1980; Hill, 1980), activated by kinetin proteins (Dela
Fuente and Leopold, 1968) and recycled for the biosynthesis
of lignin, which is required for the growth of new tissues (Can-
ton et al., 2005). The most important distinction between these
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two processes is that leaching results in a net loss of nutrients
from the plant, whereas NR is a form of recycling. It is the
active nature of NR that qualifies it as an adaptation rather
than just a passive process (Freschet et al., 2010; Menge et al.,
2011). The adaptive nature of NR elicits a degree of expressive
variation between various plant species, thus prompting
research into this topic.
Plants resorb relatively more of a particular nutrient, if the
lack of it is limiting to its growth (Han et al., 2013). What still
remains unknown; however, are the energetic costs of nutrient
uptake versus nutrient resorption in plants. While there have
been advances in recent years for understanding the mecha-
nisms of NR with limitation status, this area of research may
be broadened to include the components of the nutrients them-
selves (organic and inorganic), as well as lesser-studied micro-
nutrients, such as K, Ca, and Mg, and how the ratios between
these and N and P may vary with the limitation status and
competitive ability of plant communities.
III. NUTRIENT RESORPTION AMONG PLANT TISSUES
The remobilization of nutrients to different parts of a
plant’s anatomy is important to measure in order to study the
nutrient economy of an individual plant or a plant community.
Research on the senescence of plant tissues has generally
focused on foliage (Dela Fuente and Leopold, 1968; Smart,
1994; Zhang et al., 2013). Senescence may be considered a
form of programmed cell death (Humbeck, 2014) that occurs
in all areas of the plant anatomy; however, the most relevant
step in this process is the movement of nutrients within the
plant, and out of the plant, into the soil environment. The use
of a whole plant system in the context of nutrient resorption is
key in describing the nutrient economy of plant communities.
Different resorption estimates may be attained, contingent on
whether whole plant- or leaf-level measurements have been
made (Huang et al., 2012), and other aboveground tissues can
be as important as leaves in arriving at accurate estimates of
resorption (Yuan et al., 2005a).
The physical structures of plants determine the allocation of
nutrients to different tissues. For example, woody plants use
and allocate nutrients differently from grasses, forbs, and
ferns. Most studies dealing with woody plants do not measure
resorption patterns in other plant tissues apart from foliage,
because of difficulties in sampling of roots, bark, and stem tis-
sues throughout the annual cycle of woody plants. Non-woody
species have been logistically easier to use for the study of
resorption in non-foliar plant tissues (Mao et al., 2013). In the
following section of the review, we first describe the allocation
of nutrients to different plant tissues, and then compare NR
among plant tissues. Leaves, stems (or culms: supporting
structures in graminoids similar to woody plant stems), and
fine roots will serve as the three most fundamental plant com-
ponents for this review, as they represent the only plant tissues
measured for NR. It has been suggested that NR is largely
dependent on the environment in which plants grow (Freschet
et al., 2013; Zhou et al., 2014). Environmental controls will
be discussed further on in this review, as this topic may be of
particular interest in future studies that involve whole-plant
nutrient economy.
A. Leaves
Leaves represent a small fraction of the aboveground bio-
mass of woody plants, and the percentage of the total depends
on age, species, and turnover rates (Poorter et al., 2012).
Leaves are integral to carbon assimilation and photosynthetic
capacities within plant anatomies (Wright et al., 2004); how-
ever, carbon gain is maximized only if sufficient N is allocated
to leaves under optimum irradiance (Hikosaka, 2005). There is
often a trade-off between nutrient investment and leaf longev-
ity (Wood et al., 2011), which is closely related to the trade-
off between mean nutrient residence time and nutrient produc-
tivity (deAldana and Berendse, 1997; Yuan et al., 2008). For
example, the mean residence time of N exceeds that of leaf
longevity in most species (Aerts and Chapin, 2000; Marty
et al., 2009) as the resorption process allows for the continual
cycling of N in the canopy (Eckstein et al., 1999).
The resorption of nutrients occurs within leaf tissues in the
following two ways: from senescing leaves to stems and/or
roots, and from senescing, or older leaves, to newer leaves.
The distribution of leaf N varies throughout the canopy of
Quercus serrata trees contingent on the differentiation of light
as relates to their vertical structures (Ueda, 2012). Nutrients
are translocated from older, shaded leaves in the lower canopy
to newer, sunlit leaves (Smart, 1994; Saur et al., 2000; Hirose
and Oikawa, 2012). The increased xylem sap flow rate acti-
vated by nutrient demands from newer shoots between these
tissues allows for the transfer of nutrients from older to newer
leaves (Siebrecht et al., 2003). In the evergreen deciduous
trees of a Mediterranean environment, resorption occurs from
 NUTRIENT RESORPTION IN PLANTS
young leaves to other tissues at six months following leaf initi-
ation, then from mature leaves after two years, and finally
from dying leaves prior to senescence and leaf fall (Fife et al.,
2008). The nutrients from all three leaf stages translocate to
new shoots which, in turn, support new leaf production (Fife
et al., 2008). For evergreen coniferous species, nutrients are
also translocated from old or senescing foliage to new foliage
(Nambiar and Fife, 1991). Coniferous trees also remobilize
nutrients from older needles to facilitate growth in sink tissues,
such as stemwood, resulting in a positive increase in basal area
increments with the increased resorption of N and P from nee-
dles (Nambiar and Fife, 1991). This remobilization occurs fol-
lowing the growing season during senescence for over-winter
storage, which is then retranslocated in the spring to support
new growth (Helmisaari, 1992).
Although global data for leaf NR is ubiquitous, few stud-
ies have included the sampling of non-leaf plant tissues
along with leaves (Table 1). In these studies, for each life-
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form, nitrogen resorption efficiency (NRE, the proportion of
nitrogen resorbed back to live tissues prior to senescence) is
generally higher in leaves than in stems/culms or roots
(Table 1). In contrast, phosphorus resorption efficency
(PRE) is nearly identical among all tissues (Table 1). A
new avenue for study may include the mechanisms that
drive resoprtion of N, P, and others in leaves as well as in
other plant tissues. As previously mentioned, the cost of
leaf production may justify the higher NRE, but this also
has yet to be demonstrated.
B. Stems
In both woody and non-woody plants, stems serve as the
conduits between the roots, soil and photosynthetic tissues of
plants. For trees, the mass of stems increases linearly with the
entire plant (Enquist and Niklas, 2002), however stemwoods
are generally lower in nutrient concentrations as compared
with the other elements of tree aboveground biomass, such as
leaves, flowers, and fruits (Woodwell et al., 1975). Within
tree stems, there are two broad categories of tissues: stembark
and stemwood (further divided into sapwood and heartwood).
Generally, stembarks possess higher nutrient concentrations
than stemwoods (Ponette et al., 2001; Boucher and C^ote,
2002; Hagen-Thorn et al., 2004); however, their growth rates
are considerably different. For example, biomass production
in the stemwoods of Eucalyptus trees are ten fold higher than
that of stembarks, but the demands for P, Ca, and Mg are simi-
lar between the two (Laclau et al., 2003).
Sapwoods have higher concentrations of N, P, and K than
do heartwoods (Meerts, 2002). The translocation of N, P,
and K occurs during the senescence of sapwood to new
heartwood formation (Meerts, 2002), which challenged the
viewpoint of Eckstein et al. (1999), who first stated that
there is “probably no resorption from woody stems [. . .]”.
A critical distinction between stems and other plant tissues
475
is that the rate of senescence is much lower in these struc-
tures, whereas leaves and roots senesce over the course of a
few months to a few years (Yuan and Chen, 2010b; 2012a).
The PRE in stems or culms is similar to that of leaves for
all life forms, whereas NRE is lower in stems than leaves,
particularly for woody plants (Table 1). One possible expla-
nation for the lower NRE may be a higher priority alloca-
tion of P to new stem growth, whereas N uptake from soils
may be sufficient for woody plants to facilitate new stem
growth. On the other hand, P-limitation may create a higher
degree of PRE in stems, simply due to low availability in
soils (Yuan and Chen, 2015b).
C. Fine Roots
Nutrient dynamics within fine roots are often limited by
available technology for use in experimentation. Root turnover
patterns drive nutrient cycling (Aerts et al., 1992) and are
strongly influenced by the environment (Vogt et al., 1986;
Gill and Jackson, 2000; Yuan and Chen, 2010b), stand devel-
opment (Yuan and Chen, 2012a), and the origin of stand initi-
ating disturbances (Yuan and Chen, 2013). The relationship
between fine root biomass and resource availability governs
growth responses in these tissues. The production of fine roots
is influenced by available N and P in soils (Yuan and Chen,
2012b). For instance, northern Pinus sylvestris individuals
allocate more N to their roots than those of the same species in
southern, more fertile environments due to increased competi-
tion for soil resources in cooler, northern environments
(Meril€a et al., 2014).
Nutrient resorption in senescing fine roots was originally
thought to be negligible compared with that of foliage and
other tissues (Gill and Jackson, 2000; Gordon and Jackson,
2000). An overall 20% decrease in N concentrations was found
following senescence in the roots of four deciduous trees sub-
sequent to correcting for mass loss (Kunkle et al., 2009),
which suggests that roots do retranslocate nutrients prior to
senescence. Values for NRE in the roots of previous studies
ranged from ¡8.4% (accretion) in a Fagus sylvatica L. stand
(Van Praag et al., 1988), to 48% in a Picea abies stand
(Ahlstr€om et al., 1988), corrected for mass loss by Kunkle
et al. (2009). Nutrient resorption in the senescing fine roots of
subarctic perennial plants appears to be significant: up to
75.2% NRE and 79.8% PRE in the sedge Carex rostrata (Fre-
schet et al., 2010) (Table 1). In comparison with leaves, how-
ever, the scarce data on root nutrient resorption makes it
challenging to find any generality.
IV. CONTROLS OF GENETIC VARIABILITY
Like most plant strategies, NR is variable among plant spe-
cies (Vitousek, 1982). Plants express traits to maximize overall
fitness (Aerts and Chapin, 2000), promote growth, reproduc-
tion, dispersal, establishment and/or persistence as a response
 Downloaded by [Universite Laval] at 20:27 30 October 2015

476
TABLE 1
Nitrogen resoption efficiency (NRE, %) and phosphrous esorption efficiency (PRE, %) by plant life form for leaves, stems/culms, and roots
NRE (%) PRE (%)
Plant life form Leaves Stems/culms Roots Leaves Stems/culms Roots Source

Woody deciduous 70.2 § 3.9 (12) 35.2 § 4.5(12) 19.3 § 16.2 (2) 59.0 § 6.6 (12) 44.9 § 5.3 (12) 61.8 § 2.7 (2) Freschet et al. (2010)
Woody evergreen 62.7 § 4.4 (4) 23.3 § 5.7 (4) 13.3 § 10.3 (2) 65.7 § 3.4 (4) 44.1 § 5.0 (4) 48.1 § 16 (2) Freschet et al. (2010)
Graminoids (n D 10) 69.8 § 2.9 (10) 52.9 § 6.3 (10) 75.2 (1) 74.5 § 3.1 (6) 66.8 § 5.3 (1) 79.8 (1) Aerts and de Caluwe (1989),
Freschet et al. (2010),
L€u et al. (2012),
and Mao et al. (2013)
Forbs 63.2 § 5.9 (15) 55.9 § 4.4 (15) 28.1 § 9.8 (4) 58.7 § 6.9 (15) 65.7 § 5.4 (15) 59.1 § 5.9 (4) Freschet et al. (2010)
Ferns (n D 4) 57.8 § 18.0 (4) 66.4 § 9.3 (15) 22.1 § 13.6 (2) 78.3 § 3.4 (4) 54.1 § 17.9 (15) 44.4 § 26.4 (2) Freschet et al. (2010)
Overall 65.8 § 2.8 47.1 § 3.0 27.0 § 6.8 63.3 § 3.4 55.7 § 3.4 56.8 § 5.5
Note. Values are mean § s.e.m. The number of observations is in brackets.
 NUTRIENT RESORPTION IN PLANTS
to abiotic and biotic environments (Kattge et al., 2011). Traits
that facilitate nutrient mobility are becoming increasingly rec-
ognized for their roles in biogeochemical cycles (Wright et al.,
2004; Ordonez et al., 2009). In this section, we differentiate
NR among plant life-forms and leaf habits.
A. Variation among Plant Life-Forms
Competitive capacities among plant functional types are
strongly correlated with nutrient acquisition and utilization,
dependant on the environment (Hebert et al., 2011; Menge
et al., 2011). Within a given species, Chapin and Kedrowski
(1983) and Pugnaire and Chapin (1993) have claimed that NR
in nutrient-poor soils is not adaptive, but rather, a phenotypic
reaction to changes in the availability of nutrients in soils,
much like the passive adjustment of water uptake and use in
variable moisture conditions. Variations in NR between plant
species and between plant functional groups are, however,
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presently believed to be adaptive and non-random. In utilizing
woody and non-woody species from different clades in the
autotrophic sections of the updated Tree of Life (Cornelissen
and Cornwell, 2014), it was found that the NR of plants
located in N-limited environments is closely related to the effi-
ciency of tissue conductance for the transfer of the nutrients
(Lang et al., 2014). Although woody plants are the functional
group for which there is the most published data on nutrient
resorption, there has been an increased focus on graminoids
and forbs (Soudzilovskaia et al., 2007; L€ u et al., 2011; L€u
et al., 2012). The differentiation of NR among species groups
may therefore be a function of both non-random selection, for
nutrient conservation, and the functional traits that allow for
this process to occur. Woody and non-woody plants will be
discussed separately.
1. Woody plants
Growth in woody plants depends on relatively higher carbon
assimilation than in non-woody plants, and plant nutritonal
investments strongly correlate with biomass production
(McGroddy et al., 2004). Wood production is costly (Ryan
et al., 1996), and there is a longer mean residence time of car-
bon within the fine roots of trees than in the fine roots of
grasses (Chen and Brassard, 2013; Solly et al., 2013), which
suggests a higher degree of storage capacity, recycling, and cel-
lulose formation in woody plants. Further, the leaves of woody
plants typically have a lower leaf N and P concentrations than
non-woody species (Yuan and Chen, 2009b; Ordonez et al.,
2010; Sardans and Penuelas, 2013). These observations suggest
that the investment of energy and resource acquisition for bio-
mass production in roots of woody plants is higher than that
for non-woody plants, as structural support elements demand
higher allocations of energy (Yuan et al., 2011).
As previously mentioned, NRE is typically higher for
leaves than other tissues in woody plants, and the resorption of
477
N in stems and roots in this functional group are lower than in
non-woody plants, as demonstrated by Freschet et al. (2010)
(Table 1). The longer residence time of nutrients in the stems
and roots of woody plants likely reduces the need for NR, in
contrast to non-woody plants, whose stems and roots are rou-
tinely shed.
2. Graminoids and other non-woody plants
One of the initial studies conducted to address NR in grami-
noids was that of Aerts and de Caluwe (1989) who, by separat-
ing the plant parts following Berendse et al. (1987), found that
N and P in Molina caerulea were resorbed from senescing
leaves and culm structures into the basal internodes for over-
winter storage. The root mass fraction is higher in grasslands
than other biomes (Poorter et al., 2012), and these below-
ground tissues serve as reservoirs for future growth. Green
leaf N concentration tends to be higher in forbs than grami-
noids (L€u and Han, 2010). However, the leaf NRE of grami-
noids is higher (58.5%) than forbs (41.4%) and evergreen
woody plants (46.7%), and the PRE of graminoids is higher
(71.5%) than forbs (42.4%) and both evergreen (54.4%) and
deciduous (50.4%) woody plants (Aerts, 1996). Differences in
biomass and nutrient allocation to leaves and overall produc-
tivity may explain the higher NR in graminoids (Aerts and
Berendse, 1989), as leaf mass loss is similar between grami-
noids (8–28%; G€usewell, 2005) and woody plants (3–37%)
(van Heerwaarden et al., 2003). Tissue longevity and storage
may therefore be primary contributors to variation in NR
among plant life-forms.
Ferns tend to have similar N resorption proficiencies to
other non-woody plants, but P resorption proficiencies appear
to be lower (Killingbeck et al., 2002), indicating that ferns
contribute more P back to the soil via litterfall. However, PRE
in the winter-deciduous fern, Athyrium distentifolium, was
higher than NRE under ambient conditions in a fertilization
experiment (Holub and Tuma, 2010), suggesting that this fern
resorbs more P than N prior to senescence. Both NRE and
PRE were similar between the ferns, Dennstaedtia punctilob-
ula (winter-deciduous) and Polystichum acrostichoides (win-
tergreen; Minoletti and Boerner, 1993; Killingbeck et al.,
2002), suggesting that functional form may have a stronger
role in NR than leaf longevity in this plant functional group.
These studies represent very few that examine resorption pat-
terns in ferns; additional research is required for this functional
group to discern potentially broader trends in nutrient
resorption.
B. Role of Leaf Habit
Plant nutrient use and NR are variable with season
(McHargue and Roy, 1932; Chapin et al., 1980; Milla et al.,
2005; Niinemets and Tamm, 2005), leaf longevity (Jonasson,
1989; Escudero et al., 1992; Eckstein et al., 1999), and length
 478 A. N. BRANT AND H. Y. H. CHEN
of leaf abscission period (del Arco et al., 1991). Evergreens
are highly specialized plants, which have likely evolved an
adaptive strategy to colder and nutrient-poor soil conditions
(Reich et al., 1992), where extended leaf lifespans have
allowed for a maximized growth rate (Reich et al., 1997b),
and minimal nutrient losses that occurred during senescence
and leaf shedding (Aerts, 1995). Deciduous species exhibit
higher levels of leaf production during a growing season and
leaves are shed annually (Aerts and Berendse, 1989; Reich
et al., 1997a). Therefore, deciduous plants tend to allocate
higher quantities of nutrients to facilitate faster growth for
competitive advantage during shorter growing seasons in tem-
perate environments, whereas evergreens are slow-growing,
tolerant to harsh conditions, and have extended leaf longevity.
In deciduous plants, NR occurs from live foliage to woody
tissues for storage prior to abscission, whereas in evergreen
plants, NR occurs from older or senescing foliage to younger
foliage (Chapin and Kedrowski, 1983; Nambiar and Fife,
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1991). Although informative, estimates of resorption can be
misleading, in that nutrient-use varies widely between the two
groups. Deciduous fitness is contingent on NR since a great
deal of energy is invested into the process with a high invest-
ment in green leaf nutrients over the growing season. These
nutrients must be returned to storage tissues following senes-
cence, or the entire nutrient economy will be compromised.
For example, when resorption was prevented in Quercus ilici-
folia, stem and foliar growth declined (May and Killingbeck,
1992).
Deciduous broadleaves have a higher NRE than evergreens,
but only a slightly higher PRE (Tang et al., 2013), contradic-
tory to findings by Killingbeck (1996) and Yuan and Chen
(2009b). Plant functional type contributes more to the varia-
tion in resorption of N than climate and soils, while climate
and soils contribute more to the variation in resorption of P
(Tang et al., 2013). This leads to a further discussion as to
how plants with evergreen and deciduous leaf habits obtain
and utilize both N and P. In a similar Mediterranean climate
with a similar soil type, leaf N concentration and aboveground
biomass in evergreen tree species was higher in comparison
with deciduous species (Sardans and Penuelas, 2013); the find-
ings for biomass were contradictory to those arrive at by
Gower et al. (2001) for boreal ecosystems. From these studies,
evergreens appear to conserve high N concentrations for lon-
ger periods in the foliage, while deciduous plants contain rela-
tively less N during the growing season and retranslocate
more prior to senescence.
While it may appear that leaf N is consistently higher for
evergreens, longevity plays a strong role in the residence time
of N. The cumulative use of N in the leaves of deciduous trees
throughout their lifetime is likely much greater than that of
evergreen trees. The study of cumulative nutrient use and NR
for both evergreens and deciduous plants may therefore pro-
vide additional information than observations within a single
year, or one growing season.
V. CONTROLS OF TIME AND PLANT DEVELOPMENT
The establishment and persistence of plants throughout eco-
system succession influences soil properties, which in turn
facilitates continued growth and plant community nutrition
(Jenny, 1941). Soil profile development allows for nutrient
storage capacity, however, secondary succession may alter
soil nutrient availability. As a result, natural systems experi-
ence fluctuations of nutrient capital associated with distur-
bance (Vitousek and Reiners, 1975; Shrestha and Chen, 2010;
Chen and Shrestha, 2012). Litter N and P decreased in woody
plants of New Zealand along a soil chronsequence, from 60 to
120,000 years, thereby increasing the resorption proficiency
of N and P within older, infertile soils (Richardson et al.,
2005).
As perennial plants age, a number of processes govern both
the allocation and use of resources for growth. The shoot to
root ratio for biomass allocation increases in non-woody
perennial plants (Wilson, 1988) and decreases in woody plants
(Poorter et al., 2012; Costa et al., 2014) as they age. Above-
ground net primary production (ANPP) in individual trees
increases with age, attains a threshold level, and then
decreases (Gower et al., 1996; Ryan et al., 1997), as does fine
root production (Yuan and Chen, 2012a). The nutrient alloca-
tion to plant tissues shifts from foliage to woody tissues as
trees age (Vitousek and Reiners, 1975), where trees may allo-
cate considerably more biomass to stemwood as tree sizes
increase (Stephenson et al., 2014). These changes in biomass
and energy allocation ultimately alter nutrient demands.
The effects of time since disturbance on NR are under-stud-
ied. Leaf N and litter N concentration were observed to
increase, whereas NRE decreased with time since fire in the
decidous broadleaf Populuts tremuloides, from 68.5% NRE in
7-year-old stands to 58.4% NRE in 139-year-old stands (Yuan
and Chen, 2010a). A contrasting trend was found by Yang and
Luo (2011), where the C:N ratio in plant tissues (especially
coniferous trees) increased with stand age, but remained con-
stant in litter. These results, paired with those of Yuan and
Chen (2010a), suggested that younger trees are more N-lim-
ited, if NR is proportional to nutrient limitation (Kobe et al.,
2005). Similar results have been reported by Li et al. (2013)
for Caragana microphylla and Ye et al. (2012) for Casuarina
equisetifolia. All of these studies found negative relationships
between available N and P in soils, and NRE and PRE with
age. Therefore, both soil fertility and plant growth rates associ-
ated with time since disturbance may play roles in plant NR.
One of the primary drivers for the variable allocation of
resources is the reproductive stage, which may explain the
trends observed for stand age and NR. The generation of
reproductive tissues in the aquatic plant Sagittaria graminea,
increased as the availability of N and P in soils increased, with
soil N having a higher influence on the production of flowers
subsequent to N and P fertilization (Zhang et al., 2014).
Although nutrient-dependent reproduction in plants is not a
new concept (Harper, 1967; Harper and Ogden, 1970; Van
 NUTRIENT RESORPTION IN PLANTS
Andel and Vera, 1977), it does inspire questions regarding NR
patterns with reproductive stages. Many authors suggest that
in low-nutrient soil conditions, plants allocate more energy
and resources into growth, and less into reproductive efforts
(Liu et al., 2009), although in some cases stress may induce
flowering and fruit production (Pigliucci and Schlichting,
1995).
The nutrients required for reproduction in plants derive
from three basic sources: uptake from soil, retranslocation
from older structures, and resorption from senescing tissues
(Chapin et al., 1990; Ashman, 1994). Reproductive efforts
may place different demands on nutrient uptake and use. Prior
to fruit set, N and P were seen to decrease in the leaves, stems,
petioles, and rhizomes

of a dioecious perennial herb, Rubus
chamaemorus (Agren, 1988), and when NR was prevented in
Quercus ilicifolia, acorn production declined (May and Kill-
ingbeck, 1992). Similar findings have been revealed by Karls-
son (1994) for branch N in Rhododendron lapponicum, leaf N
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in Mangifera indica (Urban et al., 2004), and leaf K and stem
P in Dryobalanops aromatica (Ichie and Nakagawa, 2013).
All of these authors have suggested that the nutrients were
translocated to reproductive structures during these stages,
causing nutrient declines in non-reproductive structures. The
most recent study to address the role of NR in reproductive
efforts was Tully et al. (2013) who found that leaf PRE is
highest at intermediate seed counts in intermediate soil fertility
in Pentaclethra macroloba of Costa Rica. This finding sug-
gests that reproductive efforts, along with soil fertility, may
explain NR variations. This introduces a new dimension to the
measurement of plant NR, which has been overlooked in the
past, where biological events may play significant roles in
nutrient dynamics.
VI. ENVIRONMENTAL CONTROLS
It has been found that environment influences NR; in some
cases, even more so than genetics (Agren and Weih, 2012).
Foliar nutrient information has guided researchers in the deter-
mination of the overall nutritional status of an ecosystem for
over four decades now (Van den Driessche, 1974). However,
it has only been in recent years that interest has shifted from
using plant foliage to assess ecosystem quality, to estimating
the relative influence of the environment on foliage. In this
section, we divide environmental controls on NR between cli-
mate and soil.
A. Climate
1. Latitude and climate variables
Latitude is commonly used as a predictor variable for plant
nutrient cycling patterns and productivity. Between tropical
and temperate forests, N limitation is comparable (LeBauer
and Treseder, 2008); however, the relatively higher abundance
of N fixers in the tropics than temperate forests has made this
479
limitation more complex (Hedin et al., 2009). Along a global
latitudinal gradient, N limitations for productivity appear to
increase from low to high latitudes (Yuan and Chen, 2012b);
however, it is more often P limitation that differentiates the
tropics from temperate ecosystems, due to the advanced soil
age and decreasing P deposition from lack of glaciation at
lower latitudes (Elser et al., 2007). A positive relationship
exists between latitude and N and P resorption, as well as lati-
tude and leaf N and P (Oleksyn et al., 2003; Reich and Olek-
syn, 2004). This pattern may be attributed to temperature-
controlled restrictions on plant and soil biochemistry, as well
as the differences in the limitation status of both N and P in
different geological zones. Similarly, Lovelock et al. (2007)
reported that PRE and P photosynthetic use efficiency (units
of P used to perform photosynthesis) were decreased with
increasing latitude in mangroves, suggesting that plants in the
tropics have evolved under historically low P availability. On
a smaller scale, Tang et al. (2013) found a general increase in
NRE and decrease in PRE with increasing latitude in eastern
China for different functional plant groups.
Climate is a primary driver in NR. Within four plant groups
(trees, shrubs, conifers, and broadleaves), NRE decreased with
increasing mean annual temperature (MAT) and mean annual
precipitation (MAP; Yuan and Chen, 2009a), confirming the
results of Oleksyn et al. (2003). In contrast, PRE increased
with increasing MAT and MAP (Yuan and Chen, 2009a), lead-
ing to the argument of N-limitation in colder climates and P-
limitation in warmer ones (Yuan and Chen, 2012b). However,
Vergutz et al. (2012) suggested that both NRE and PRE
decrease with MAT and MAP and increase with latitude, con-
trary to the results by Yuan and Chen (2009a). This inconsis-
tency with PRE warrants further examination. Both studies
used the meta-analysis approach with a global dataset. While
Vergutz et al. (2012) used senesced data collected from litter
traps, Yuan and Chen (2009a) opted to use only freshly-
abscised leaves, which reduced the sample size but was likely
to maintain a higher level of reliability, given that leaching
may lead to an underestimation of litter concentration by up to
8% for N and 10% for P (Boerner, 1984). An underestimation
of litter nutrient concentration might result in an overestima-
tion of resorption efficiency, which does explain the lower
PRE for climates with higher MAP, found by Vergutz et al.
(2012), given that rainfall is the primary driver of nutrient
leaching from leaves at low latitudes. This inconsistency
emphasized the importance of choice of methodology and
scaling in the study of NR.
2. Climate change
Plants with broad ecological amplitudes may be able to
buffer against climate change events such as increased CO2
concentrations, global warming, drought, N deposition, and
species invasions (Sardans and Penuelas, 2012). The pathways
for adaptation to climate change, however, are still unknown
 480 A. N. BRANT AND H. Y. H. CHEN
and have been principle topics of climate change research over
the last decade, due to our dependence on plant/forest ecosys-
tems for human sustenance (Tubiello et al., 2007), clean air
(Nowak et al., 2006), and provisions for wildlife (Doiron
et al., 2014).
Climate change affects the nutritional stoichiometry of the
global plant community (Dijk et al., 2012; Dijkstra et al.,
2012; Sardans et al., 2012; Yuan and Chen, 2015a), as well as
that in soils (Delgado-Baquerizo et al., 2013). Northern envi-
ronments, which tend to be N-limited, are particularly suscep-
tible to further N restrictions under elevated CO2, since
enhanced plant growth increases mineral nutrient requirements
(Norby et al., 2010). Nitrogen is employed in plant tissues,
and is also stored in organic matter with soils following CO2
sequestration. However, N from biological and atmospheric
sources may not keep up with sources of CO2 for plant uptake
and use (Hungate et al., 2003; Luo et al., 2004; K€orner et al.,
2005; Reich et al., 2006; Norby et al., 2010). Variations in N
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metabolism among plant species may result in variable
responses of plants to CO2 enrichment (Bassirirad, 2000).
Increased aridity in global drylands due to climate change may
decrease the availability of N in soils, while increasing the
availability of P; driving changes in the soil environment and
plant communities (Delgado-Baquerizo et al., 2013). In terres-
trial plants, N:P ratio increases with warming, drought, and N
fertilization, creating a shift from N-limitation to P-limitation
in plants, whereas N:P ratio decreases with elevated concentra-
tions of CO2, increasing rainfall, and P fertilization (Penuelas
et al., 2013; Yuan and Chen, 2015a).
The effects of elevated CO2 conditions on NR was first
addressed by Norby et al. (2000) with Acer trees using open-
top chambers. Litter N was lower, i.e., high nitrogen resorption
proficiency, in the elevated CO2 chambers; however, NRE was
unaffected (Norby et al., 2000). With graminoid species under
warming and CO2-elevated treatments, their N:P ratios mea-
sured in green plant biomass were lower than in senesced plant
biomass, indicating that PRE was greater than NRE in the
studied species (Dijkstra et al., 2012). However, no effect of
summer warming was found on the NRE of Betula and Rubus
species residing in a bog (Aerts et al., 2007).
Water availability is a major factor in NR (Killingbeck,
1993), but it is inconclusive as to whether NR is directly
dependent on annual precipitation (Drenovsky et al., 2010) or
whether the onset of drought conditions elicits a response in
NR. Changes in the hydrological cycle may modify nutrient
availability, thereby altering the ability of plants to utilize
nutrients in the soil (Tomer and Schilling, 2009). The NRE
and PRE of two Mojave desert shrubs were only responsive to
elevated CO2 concentrations in a dry year (Housman et al.,
2012), suggesting that drought may be a more determinant fac-
tor in the variation of NR than atmospheric effects. Drought-
tolerant desert plants are plastic in their ability to retranslocate
nutrients, as demonstrated in Fouquieria splendens, a drought-
deciduous shrub which was inefficient in resorbing N (11%)
(Killingbeck, 1992), but three years later resorbed up to six
times the amount of N (72%) (Killingbeck, 1993). Drought-
deciduous shrubs such as these are adapted to low water envi-
ronments by way of multiple leaf production cycles in one
growing season induced by intermittent rain periods (Killing-
beck, 1992). A decrease in NRE was observed in both N-fixing
and non-N-fixing plants growing in a temperate climate over
one year, coinciding with a 7.2% increase in precipitation over
the same period (Stewart et al., 2008). Lower NRE and higher
N resorption proficiency were observed during drought condi-
tions in plants adapted to drier environments (Khasanova
et al., 2013). Resorption has been identified as a key mecha-
nism in the delay of desertification in plants during reduced
nutrient capitals of soils (Killingbeck, 1993; Li et al., 2014),
but there is still no further evidence to support this theory.
Greenhouse studies may be useful in studying NR under dif-
ferential moisture conditions (Drenovsky et al., 2010).
While there is extensive research on long-term climate
change, there is less on NR with variations in the frequency of
extreme weather events. PRE decreased significantly after a
hurricane event in Populus tremuloides, and the concentration
of N in the senesced litter was higher than the green leaf N
prior to the hurricane (Killingbeck, 1988). This study sug-
gested that severe, short-term disturbances such as hurricanes
may cause damage to ecosystem function, even in the absence
of more obvious mechanical damage. Research into the effects
of extreme weather events on NR may improve the knowledge
base for climate change modelling (Thompson et al., 2013) in
terms of droughts, floods, and other environmental disasters.
Although the focus continues to be on individual elements –
N-limitation vs. P-limitation, the most stressed consequence of
climate change on plant nutrition is in the relative ratios of the
nutrients, and how they interact with other biotic or biochemi-
cal events in ecosystems. The Stoichiometrically Coupled,
Acclimating Microbe-Plant-Soil model is one novel tool that
may assist in addressing issues surrounding co-limiting nutri-
ent dynamics under ecosystem change (Sistla et al., 2014).
The incorporation of stoichiometric relationships between
nutrients and life-forms is crucial for understanding the
impacts of climate change on plants.
B. Soil Fertility
Plant growth is nutrient-limited, and therefore a nutrient-
conserving strategy was selected for plants occupying infertile
soils (Aerts and Vanderpeijl, 1993). It has been historically
postulated that the higher NR patterns observed in evergreens
residing in bogs, in contrast to those residing in nutrient-rich
ecosystems, was a result of plant adaptation to low nutrient
availability (Small, 1972), and that NR is a reflection of the
plant nutrient status relative to the environment (Chapin,
1980). However, there is still an ongoing debate as to whether
NR is directly related to soil fertility, particularly for plants
that are adapted to low-nutrient soil conditions. Soil fertility
 NUTRIENT RESORPTION IN PLANTS
has been employed interchangeably with green leaf nutrient
status when describing NR. Originally, both Chapin (1980)
and Aerts (1996) found no relationship between green leaf
nutrient status and resorption efficiencies. The concept of soil-
NR relationships was re-assessed using the available literature,
where 32% of the studies revealed a decrease in NRE, and
35% resulted in a decrease in PRE with increased soil fertility
(Aerts, 1996; Aerts and Chapin, 2000). The debate for existing
soil-NR relationships was then set aside when 63% of studies
supported the null response of NR to soil nutrient fertility
(Aerts and Chapin, 2000). More recently, Kobe et al. (2005)
found evidence using a global dataset to support the negative
relationship proposed between NRE and green leaf N and P,
which was later corroborated by Vergutz et al. (2012).
It remains imperative to employ natural gradients of nutri-
ent availability to elucidate the relationship between NR and
nutrient availability, particularly for large, long-lived plants
such as trees (Drenovsky et al., 2013; Tully et al., 2013;
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Campo et al., 2014; Hayes et al., 2014). Fertilization experi-
ments, on the other hand, provide direct tests for the effects of
nutrient availability on NR in natural environments (L€u et al.,
2013; Mao et al., 2013; Mayor et al., 2014; Wang et al.,
2014), and greenhouse experiments (de Campos et al., 2013).
Experimental studies may also examine whether the influences
of multiple factors on NR are additive (Holub and Tuma,
2010). The addition of N, P, and other macronutrients using
different ratios have the effect of altering NR in plants (Wang
et al., 2014), and the addition of N may cause a decline in
green leaf P and K (Goodman et al., 2014), emphasizing the
importance of stoichiometric relationships between nutrients
in the soil (Agren and Weih, 2012). A recent global meta-anal-
ysis of nutrient fertilization experiments has indicated that
increased soil fertility reduces both NRE and PRE (Yuan and
Chen, 2015b).
The relative costs associated with resorbing materials back
into live tissues from senescing ones, in comparison to nutrient
uptake from soils is currently unknown. However, the optimi-
zation of NR, relative to leaf longevity and nutrient storage,
has been described (Field, 1983; Chapin et al., 1990). The N
response efficiency (biomass production per unit N in the soil)
was shown to increase as a response to decreasing N availabil-
ity in the soil, which is closely tied to N uptake efficiency
(Yuan et al., 2006). This knowledge gap of how NR relates to
soil nutrient capital as a function of energy optimization might
serve as one of many future research efforts.
VII. SUMMARY AND FUTURE PERSPECTIVES
1. Nutrient resorption (NR) is the remobilization of nutrients
from senescing or older tissues to storage structures, or
newer tissues in plants. Global estimates for leaf N resorp-
tion efficiency (NRE) and P resorption efficiency (PRE) are
62% and 65%, respectively.
481
2. NR also occurs in stems, culms, and roots, but to a lesser
degree than in leaves. NR from senescing roots may be
greater than that from leaves; however empirical evidence
in non-leaf tissues is scarce.
3. Genetic variability among plants impacts NR, which in
woody plants, is typically lower in senescing stems and
roots than non-woody plants. Non-woody plants exhibit
enhanced plasticity in their expression of NR along soil fer-
tility gradients.
4. Evergreen species, due to their long leaf lifespans, possess
lower NR than deciduous plants. Nutrient residence time is
higher in evergreens than deciduous species whose nutrient
cycling is more dependent on NR.
5. Along a soil chronosequence over large temporal scales
(thousands of years), NR increases to accommodate older,
infertile soils. NR in trees decreases with stand develop-
ment, which is attributable to a lower demand for nutrients
with lower growth rates in older trees; however, this obser-
vation may often be confounded with increasing soil fertil-
ity over time. NR increases during periods of the high
generation of reproductive structures due to elevated nutri-
ent demands.
6. PRE increases and NRE decreases with increasing tempera-
ture and precipitation, although there are discrepancies in
the literature. Variations in nutrient availability between
differing substrates along latitudinal gradients may explain
this trend.
7. Extreme weather events such as droughts, floods, and hurri-
canes may significantly influence NR. Evidence for the
effects of long-term climate change (CO2 enrichment,
warming and altered precipitation) on NR is limited.
8. Both observational and experimental studies indicate that
increasing soil fertility tends to lower NR.
The responses of plants to environmental changes involve
regulatory pathways that we are only beginning to understand.
The unravelling of the mechanisms for NR in plant communi-
ties is important toward better understanding ecosystem func-
tion, health, and resilience to change. Much more data will be
required about NR in non-leaf tissues in order to understand
the process at both the whole plant and ecosystem levels. This
topic may be of particular interest in future studies that deal
with whole-plant nutrient economy. Variations in NR among
leaf habits also raises questions as to how nutrient cycling is
affected by compositional shifts in vegetation that result from
succession in plant communities. Future research efforts on
how NR changes with leaf habit are likely to aid with the fore-
casting of global changes in nutrient ecosystem economies.
The influences of plant age on NR, particularly in trees, are
under-studied. Future research might include patterns of NR in
old-growth forests, as well as grasslands, which comprise a
large portion of the global vegetative cover. Older plant com-
munities may serve as either nutrient reservoirs for future gen-
erations, or may be under the stress of nutrient limitations. In
 482 A. N. BRANT AND H. Y. H. CHEN
addition to ecosystem age, the incorporation of reproductive
stages in NR measurements may also improve estimate accu-
racies, given that they contribute a great deal of variation in
energy allocation.
While the findings of the effects of climate change (specifi-
cally CO2 enrichment and warming) on NR are currently
inconsistent, abrupt changes in weather patterns might reveal
interesting plant responses. The incorporation of stoichiomet-
ric relationships between nutrients and life forms is crucial for
the study of climate change mitigation and monitoring. While
much is known about the capacities of plants to retranslocate
materials to living elements in the prevention of nutrient loss,
there remains much yet to be explored. Under a changing cli-
mate, plant communities at the global scale experience
changes that are challenging to accurately predict. Improving
our understanding of how plants express NR may supplement
global climate change models, especially those that concern
biogeochemical parameters.
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ACKNOWLEDGMENTS
We thank Samuel Bartels, Eric Searle, Zhiyou Yuan, Dave
Morris, Rongzhou Man, and anonymous reviewers for their
valuable comments on an early version of the paper. Financial
support from the Natural Sciences and Engineering Research
Council of Canada (DG281886-09 and STPGP428641) and
the Early Researcher Award from the Ontario Ministry of
Research and Innovation (ER-07-04-062) is gratefully
acknowledged.
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